Skin impulse excitation of spinal sensory neurons in developingXenopus laevis(Daudin) tadpoles

Abstract

SUMMARYResponses to gentle touch in young Xenopus tadpoles are mediated by spinal cord sensory Rohon–Beard neurons. Tadpoles also respond to noxious stimuli that elicit ‘skin impulses’, which propagate between epithelial cells over the whole body surface, somehow entering the CNS to generate a response. After hatching (∼48 h post-fertilization), skin impulse signals enter the CNS only via cranial nerves, but previous evidence suggested the possibility of direct entry to the spinal cord before this (∼24 h). We have used behavioural and electrophysiological methods to explore the developmental pattern of skin impulse entry into the spinal cord and the involvement of Rohon–Beard neurons. Lesioning confirmed that skin impulse signals can directly enter the spinal cord in young embryos, but access decreases over ∼12 h and disappears soon after hatching. Electrical recordings from central Rohon–Beard axons in young embryos showed firing in response to skin impulses. However, unit recordings from Rohon–Beard somata showed that individuals that responded to touch within a characteristic, localised receptive field did not fire to skin impulses, whereas others from similar locations responded reliably. Developmental loss of skin impulse access to the spinal cord mirrored the known spread of sensitivity to gentle touch as the peripheral mechanosensory endings of Rohon–Beard neurons mature. Together, these results suggest that Rohon–Beard neurons respond to skin impulses only while immature, providing a transitory route for skin impulses to excite the CNS. In this way, Rohon–Beard neurons would mediate responses first to noxious and then to localised, gentle touch stimuli as the neurons developed.